Transverse openings on some cervical vertebrae of children buried in the mid-Upper Paleolithic site of Sungir (Sungir 2 and 3) are unclosed and doubled. Non-closure is observed in both children on C1, in one (Sungir 3) also on C4 and C5. In child Sungir 2, there was a doubling of holes on C4 and C6, and in child Sungir 3 - on C4 - C6. Such a combination is very rare in modern people. The relationship of these features with the variants of blood vessels is unclear, so it is difficult to give them any interpretation.

Key words: vertebrae, transverse foramina, vertebral artery, Upper Paleolithic, paleopathology, paleoanthropology.

Introduction

When examining the vertebrae of children's skeletons 2 and 3 from the burial site of the middle pore of the Upper Paleolithic Sungir, a number of anomalies of the transverse openings of several cervical vertebrae were found. Since the transverse openings of at least the first six cervical vertebrae (C1 - C6) normally form around the vertebral arteries during ontogenesis and are thus associated with the vital arterial blood supply to the brain, their variability deserves attention. The lateral parts of some transverse openings on the cervical vertebrae were not closed, and in several cases there are two openings on each side instead of one. The latter anomaly was noted in the literature (Anderson, 1968; Taitz, Nathan, Arensburg, 1978; Jovanovic, 1990; Das, Suri, Kapur, 2005), but without taking into account its unilateral or bilateral occurrence and the degree of formation of the entire cervical spine.

Material and methods

Sungir 2 and 3. The skeletons of children come from a double burial site excavated in 1969 at the Sungir site near Vladimir (Bader, 1978, 1998). They were lying with their skulls facing each other. According to the results of direct radiocarbon dating by accelerator mass spectrometry, the skeletons are 26-30 thousand years old (calibrated dates are 34-31 thousand years ago) [Kuzmin et al., 2004; Dobrovolskaya, Richards, and Trinkaus, 2012; Marom et al., 2012]. The mixed composition of fauna and flora with a predominance of cold-tolerant species and some more heat-loving ones (Alekseeva, 1998; Lavrushin, Sulerzhitsky, and Spiridonova, 2000), as well as the nature of fossil soils (Gugalinskaya and Alifanov, 2000) indicate that the site belongs to one of the interstadials within the MIS-3 interplanetary zone (Ibid.Most likely, to the fifth, whose radiocarbon date is about 28 Ka BP [Svensson et al., 2008]. This allows us to date the burial to the beginning of the Middle stage of the Upper Paleolithic of Eastern Europe.

Given that Sungir is an open-type Upper Paleolithic site, the preservation of both children's skeletons should be considered exceptionally good. Only the distal end of the humerus (Sungir 2) is missing. The degree of ossification of the dental crowns allowed us to conclude that one child was 11-13 years old (Sungir 2), the other 9-11 years old (Sungir 3) [Mednikova, Buzhilova, Kozlovskaya, 2000; Guatelli-Steinberg, Buzhilova, Trinkaus, 2011]. Senior's gender -

page 126
male, younger-probably female (Poltoraus, Kulikov, Lebedeva, 2000; Mednikova, Buzhilova, Kozlovskaya, 2000).

The burial site is widely known mainly due to the exceptional wealth of inventory [Bader, 1998], as well as the abnormal structure of the femur bones in the Sungir 3 child, along with pronounced symptoms of nonspecific stress [Bukhman, 1984; Buzhilova, 2000; Mednikova, 2000; Formicola and Buzhilova, 2004; Buzhilova, 2005; Guatelli-Steinberg, Buzhilova, Trinkaus, 2011]. Anomalies of the axial skeleton in Sungir children have not yet been described. Both had hypertrophy of the limb bones, reflecting the level of physical activity typical for the Upper Paleolithic hunter-gatherer population (Mednikova, 2000; Cowgill et al., 2012).

In both individuals, all seven cervical vertebrae were preserved; only some transverse processes and metaphysical ends of spinous processes were damaged (Figs. 1, 2). The structure of the transverse openings of the cervical vertebrae was studied by us in the Plastic Reconstruction Laboratory of the Institute of Anthropology and Ethnography of the Russian Academy of Sciences in Moscow with the permission of T. S. Baluyeva.

Up-to-date material used for comparison. To assess the normal variability of transverse foramina in modern children, we studied the structure of the cervical vertebrae, on both sides of which the closure/non-closure of the lateral parts of the foramina was determined, and the presence of additional foramina was recorded. In addition, we noted the complete absence of holes; such cases are rarely found in modern adults (Taitz, Nathan, Arensburg, 1978; Jovanovic, 1990; Vasudeva, Kumar, 1995).

The sample consists of 69 mostly complete sets of cervical vertebrae from the Indian Knowle Archaic burial ground ("Indian Mound", Kentucky, USA), which is 4-5 thousand years old (Libby, 1955; Webb, 1974). In this Native American paleopopulation, it is quite well represented-

Fig. 1. Cervical vertebrae of the Sungir 2 child (top view).

2. Cervical vertebrae of the Sungir 3 child (top view).

page 127
children and teenagers are involved. Vertebrae with significant pathological changes were excluded from consideration. Since the transverse openings are normally completely closed by 3-4 years [Scheuer, Black. 2000], we limited the sample to the age range of 6-16 years to ensure comparability with the Sungir material.

Since we are talking about a series of archaeological sites, not all individuals are represented by a complete set of cervical vertebrae, and on some vertebrae, the transverse openings are not available for study on both sides or on one. The total number of cases was as follows: C1-56, C2-57, C3 - 57, C4 - 56, C5 - 53, C6 - 56, C7 - 53.

Methodology. The transverse opening was considered open if there was a clear gap between the anterior (ventral) and posterior (dorsal) parts of the arch around it. Non-closure was recorded if the bone edges of the arch are formed by a compact layer (otherwise, a postmortem defect cannot be excluded). It is likely that open holes are more susceptible to failure, but since this is not proven, holes with defects were not taken into account. Doubling was observed in the presence of a clearly defined additional hole with a diameter of at least 1 mm on at least one side of the vertebra.

Results

Modern children. In a small number of cases (one for C2, C3 and C7, two for C6 and three for C5), the absence of a transverse opening on one side of the vertebra was observed. When calculating the occurrence of open and double holes, these cases were not taken into account.

Open openings are most frequent in the Atlas (Table 1).They occur more than twice as often in the epistrophaea, and no more than once in each of the other five cervical vertebrae (never in C7). Thus, unclosed transverse foramina are quite common on the Atlas and epistrophaea, but rare on the rest of the cervical vertebrae.

The distribution of additional holes is opposite (Table 1). They have never occurred on the first two cervical vertebrae, are occasionally observed on C3 and C4, and on the other three are very frequent, in particular, on C6 (right side) and C7 (left side) are observed in almost every third case.

If an additional transverse hole is present on at least one side, then in 41.1 % of cases it is also noted on the other (N = 56, only vertebrae with both sides preserved were taken into account). Similarly, in a smaller group of vertebrae with an open opening on at least one side, the occurrence was bilateral in 41.2% of cases (N = 17). So, these options can not be called either symmetric or asymmetric.

Sungir 2 and 3. In both Sungir children, some transverse openings of the cervical vertebrae are unclosed (Table 2). In particular, in the Sungir 2 child, as in many modern children, non-closure is observed on the atlas on both sides and on the epistrophaea on one side, while on the other vertebrae all the openings are closed. In child Sungir 3, this anomaly is noted not only on the atlas (on both sides), but also on three other cervical vertebrae - C4, C5 (on one side) and C6 (on both sides).

In both children, doubling of the holes, at least one-sided, was noted on C6, and in the Sungir child 3 and on C5 on both sides (Table 3). At the co-

Frequency of unclosed and doubled transverse openings of the cervical vertebrae in a near-modern series of skeletons of children aged 6-16 years from the Indian Knowle Indian burial ground (Kentucky, USA), Table 1. %

Vertebra

Unclosed

Extension service

On the right

Leftward

On the right

Leftward

C1

18,2(43)

14,6(41)

0(53)

0(54)

C2

8,2 (49)

6.1 (49; 1 ots.)

0(56)

0(56)

C3

2,2 (45)

2.1 (48; 1 ots.)

3,6 (56)

1,8 (56; 1 ot.)

C4

2,0 (49)

0(39)

5,7 (53)

3,8 (53)

C5

2,4 (42; 1 ot.)

2.6 (38; 2 ots.)

23.1 (52; 1 ots.)

15.7 (51; 2 ots.)

C6

3,3 (30)

3,4 (29; 2 ots.)

35,2 (54)

23.1 (52; 2 ots.)

C7

0 (28; 1 ots.)

0(28)

15.4 (52; 1 ot.)

31,4(51)

Note: the total number of observations and the number of cases of missing holes are shown in parentheses.

page 128
Table 2. Non-closure of transverse openings on the cervical vertebrae of Sungir children

Vertebra

Sungir 2

Sungir 3

On the right

Leftward

On the right

Leftward

C1

+

+

+

+

C2

+

-

-

-

C3

-

(-)

-

-

C4

-

(-)

+

-

C5

-

(-)

+

-

C6

-

(-)

+

+

C7

-

?

-

?

Note: in parentheses, information about cases where the bone is damaged, but the sign is still available for observation.

Table 3. Doubling of transverse openings on the cervical vertebrae of Sungir children

Vertebra

Sungir 2

Sungir Z

On the right

Leftward

On the right

Leftward

C1

-

-

-

-

C2

-

-

-

-

C3

-

-

-

-

C4

+

-

-

+

C5

-

-

+

+

C6

+

+

+

-

C7

-

?

?

?

in children, additional holes on these vertebrae are also not uncommon. But the Sungir ones also have them on C4 (on the one hand), which is rare in modern humans.

Discussion

Transverse openings of the cervical vertebrae in modern humans. The absence of transverse foramina and their doubling in modern series was repeatedly noted. S. Das and co-authors found right-sided doubling in 1.5% of cases, and left-sided doubling in 0.8 % (N = 132 vertebrae, more precise data are not available) [Das, Suri, Kapur, 2005]. S. Taits and her colleagues noted the absence of a hole on the left vertebra. three C4s (8.3 %) and one C6 (2.8%), and doubling on at least one side was observed in 13.9% of C5s, 61.1% of C6s, and 19.4% of C7s (N = 36 individuals) [Taitz, Nathan, and Arensburg, 1978]. MS Jovanovic, after examining the 7th cervical vertebra of 42 individuals, found no hole missing. Its doubling was observed on the right in 11.9 % of cases, on the left - in 7.1 %; on two of the six vertebrae, it was bilateral (Jovanovic, 1990). So, the last two studies, in contrast to the first, showed that additional transverse holes on the lower cervical vertebrae are quite common, and the absence of holes is very rare. Thus, according to these signs (the non-closure of holes was not registered by the mentioned authors), there is a correspondence with the data on the children's and youth series from the Indian Knowle burial ground. The study of the latter leads to the following conclusions regarding the transverse hole: 1) its absence is a rare but not exceptional phenomenon; 2) non - closure is more often recorded on the upper cervical vertebrae, especially on the Atlas; 3) doubling occurs with moderate frequency, mainly on the lower three cervical vertebrae.

The anatomical meaning of the observations remains unclear. Normally, the vertebral artery passes through the transverse openings of at least the first six cervical vertebrae, along which arterial blood flows through the basilar artery to the circle of willis, as well as the vein and sympathetic nervous plexus. However, a bony ring is not always formed around the vertebral artery during ontogenesis by closing the costal and transverse processes of the cervical vertebra (Scheuer and Black, 2000). In the upper part of the cervical spine, it passes through the Atlas spinal canal (Tokuda et al., 1985), and in the lower part it is most often located outside the 7th vertebra (Jovanovic, 1990; Jitendra and Hrishikesh, 2012). It was assumed that the vertebral vein passes through the transverse foramen C7 (see, for example, Epstein, 1969; Taitz, Nathan, and Arensburg, 1978). However, as the study by M. S. Jovanovic showed, this is not the case: usually only small vessels of the ascending or deep cervical arteries and veins, as well as sympathetic nerves, pass through it (Jovanovic, 1990). Therefore, the transverse openings of the 7th cervical vertebra are formed in some other way.

The situation is complicated by the fact that occasionally (in 0.2 - 2.0% of cases) the vertebral artery is doubled or fenestrated due to the cessation of involutive development of embryonic blood vessels [Goddard et al., 2001; Ionete and Omojola, 2006; Kendi and Brace, 2009]. In the first case, the accessory artery passes outside the vertebra along the transverse process, and in the second case it can be located both inside and outside the vertebra. However, since doubling or fenestration of the artery is usually diagnosed radiographically, while the closure of the transverse opening or its doubling is determined by direct examination of the vertebra or histologically, the relationship between these phenomena remains unclear. An additional opening may indicate an additional vertebral artery, vein, or nerve (Taitz, Nathan, and Arensburg, 1978).

The absence of an opening could theoretically mean that the vertebral artery enters the cervical spine above C6. Our data, however, show that,

page 129
This interpretation is not supported, since in some cases there are no holes on the overlying vertebrae, but there are holes on the underlying vertebrae. In these cases, the vertebral artery may exit the spine, form a loop around the vertebra, and re-enter. Or, as already noted in relation to the atlas, it can enter the spinal canal through the intervertebral space. Similar arterial anomalies were observed in living people, but it is not known whether they were accompanied by the absence of a transverse opening (Wickbom and Williamson, 1980). In some cases, the vertebral artery expands towards the head. This may explain the non-closure of the transverse openings of the Atlas and Epistrophaea (Epstein, 1969). By the way, they have larger openings than the underlying cervical vertebrae (Taitz, Nathan, Arensburg, 1978).

Sungir 2 and 3. According to the three features considered, the variability of the transverse openings of the cervical vertebrae of Sungir children generally fits within the limits of variations in modern humans, although the tendencies to non-closure and doubling are very pronounced in them. The features that make Sungiris extremely variable in modern humans include the unilateral doubling of the transverse opening on C4 in both children and the openness of the openings on C4-C6 in the Sungir 3 child.

The generally similar distribution of frequencies of open and doubled transverse openings in Sungir and modern children, as well as the similarity of the latter with adults in the second feature, indicate that we are looking at normal anatomical variants that arise in the process of ontogenesis. Therefore, they are unlikely to be related in any way to the deformity of the femur bones in the Sungir 3 child or to the symptoms of nonspecific stress detected in both children [Formicola and Buzhilova, 2004; Guatelli-Steinberg, Buzhilova, Trinkaus, 2011]. However, it is impossible to exclude the correlation between the openness of the transverse openings on C4-C6 in the Sungir 3 child, which should be seen as a manifestation of the stop (incompleteness) of normal morphogenesis, and other skeletal anomalies in this individual.

Conclusion

Pronounced non-closure of the transverse openings of the cervical vertebrae, as well as their doubling at C4-C6 in Sungir children, generally do not exceed the limits of normal variations in modern humans. However, according to some features associated with these variations, the Sungir people occupy an extreme place. On the one hand, they, like modern humans, have mostly unclosed openings of the upper cervical vertebrae, but are doubled on the lower three. On the other hand, doubling on C4 and opening of the openings of at least one of the cervical vertebrae from the 4th to the 6th in the Sungir 3 child indicate the possibility of linking these features with other developmental anomalies in this individual.

Acknowledgements

We are grateful to the late T. S. Baluyeva for the opportunity to study the Sungir skeletons, as well as to A. P. Pestryakov, E. V. Veselovskaya, and N. O. Bader, who helped us. The series from the Indian Knowle Burial Ground was studied with the permission of J. R. R. Tolkien. Crothers with the help of N. O'Malley. This study is part of a project aimed at re-examining human remains from Sungir. Its participants were also A. P. Buzhilova, M. V. Dobrovolskaya and M. B. Mednikova. The project was funded by the Russian Foundation for Basic Research and the J. Washington University (USA).

List of literature

Pozdnepaleoliticheskoe poselenie Sungir ' (pogrebeniya i okruzhayushchaya sreda) [Late Paleolithic settlement of Sungir (burials and environment)], ed. by N. O. Bader, Moscow: Nauch. mir, 1998, pp. 240-257.

Bader O. N. Sungir: Upper Paleolithic site, Moscow: Nauka Publ., 1978, 271 p.

Bader N. O. Sungir: Paleolithic burials / / Late Paleolithic settlement of Sungir (burials and environment) / ed. by N. O. Bader, Moscow: Nauch. mir, 1998, pp. 5-160.

Buzhilova A. P. Analiz anomaliy i indikatorov fiziologicheskogo stressa u nepolovozrelyykh sungirtsev [Analysis of anomalies and indicators of physiological stress in immature Sungirians]. Homo sungirensis: Verkhnepaleoliticheskiy chelovek: ekologicheskie i evolyutsionnye aspekty issledovaniya [Homo sungirensis: Upper Paleolithic man: ecological and evolutionary aspects of research].

Bukhman A. I. Roentgenologicheskoe issledovanie skeletov detey verkhnepaleoliticheskoy stoyki Sungir ' [X-ray study of skeletons of children of the Upper Paleolithic Sungir site]. Moscow: Nauka Publ., 1984, pp. 203-204.

Gugalinskaya L. A., Alifanov V. M. Fossil soils of the late Pleistocene and features of the soil-forming process based on the materials of the Sungir settlement / / Homo sungirensis: Upper Paleolithic man: ecological and evolutionary aspects of research / ed. by T. P. Alekseev, N. O. Bader, Moscow: Nauch. mir, 2000, pp. 43-46.

Lavrushin Yu. A., Sulerzhitsky L. D., Spiridonova E. A. Vozrast 'arkheologicheskogo pamyatnika Sungir' i osobennosti prirodnoi sredy vremeni obitaniya pervobytnogo cheloveka [The age of the Sungir archaeological site and features of the natural environment of the time of primitive man's habitation]. Homo sungirensis: Verkhnepaleoliticheskiy chelovek: ekologicheskie i evolyutsionnye aspekty issledovaniya [Homo sungirensis: Upper Paleolithic man: ecological and evolutionary aspects of research], Moscow: Nauch. mir, 2000, pp. 35-42.

Mednikova M. B. Roentgenomorphology of children from burial 2 / / Homo sungirensis: Upper Paleolithic

page 130
Chelovek: ekologicheskie i evolyutsionnye aspekty issledovaniya [human: ecological and evolutionary aspects of research].

Mednikova M. B., Buzhilova A. P., Kozlovskaya M. V. Sungir 2 and Sungir 3: Sex and age diagnostics according to morphological criteria of the bone system / / Homo sungirensis: Upper Paleolithic man: ecological and evolutionary aspects of research / ed. by T. I. Alekseeva, N. O. Bader. - Moscow: Nauch. mir, 2000. - p. 57 - 60.

Poltoraus A. B., Kulikov E. E., Lebedeva N. A. Molecular analysis of DNA from the remains of three individuals from the Sungir site / / Homo sungirensis: Upper Paleolithic man: ecological and evolutionary aspects of research / ed. by T. I. Alekseev, N. O. Bader, Moscow: Nauch. mir,2000, pp. 351-358.

Anderson J.E. Skeletal "anomalies" as genetic indicators // Symposia of the Society for the Study of Human Biology. - 1968. - Vol. 8. - P. 135 - 147.

Buzhilova A. P. The environment and health condition of the Upper Palaeolithic Sunghir people of Russia // J. of Physiological Anthropology and Applied Human Sciences. - 2005. - Vol. 24. - P. 413-418.

Cowgill L.W., Mednikova M.B., Buzhilova A.P., Trinkaus E. The Sunghir 3 Upper Paleolithic juvenile: Pathology and persistence in the Paleolithic // Intern. J. of Osteoarchaeology. - 2012. - Doi: 10.1002/oa.2273.

Das S., Suri R., Kapur V. Double foramina transversaria: An osteological study with clinical implications // Intern. Medical! (Tokyo). - 2005. - Vol. 12, N4. - P. 311 - 313.

Dobrovolskaya M., Richards M.P., Trinkaus E. Direct radiocarbon dates for the Md Upper Paleolithic (eastern Gravettian) burials from Sunghir, Russia // Bull, et Memoires de la Societe d'Antropologie de Paris. - 2012. - Vol. 24. - P. 96 - 102.

Epstein B.S. The Spine: A radiological Text and Atlas. - Philadelphia: Lea and Febiger, 1969. - 790 p.

Formicola V., Buzhilova A.P. Double child burial from Sunghir (Russia): Pathology and inferences for Upper Paleolithic funerary practices // Am. J. of Physical Anthropology. - 2004. - Vol. 124, N3. - P. 189 - 198.

Goddard A.J., Annesley-Williams D., Guthrie J.A., Weston M. Duplication of the vertebral artery: report of two cases and review of the literature // Neuroradiology. - 2001. - Vol. 43. - P. 477 - 480.

Guatelli-Steinberg D., Buzhilova A.P, Trinkaus E. Developmental stress and survival among the Md Upper Paleolithic Sunghir children: Dental enamel hypoplasias of Sunghir 2 and 3 // Intern. J. of Osteoarchaeology. - 2011. - Doi: 10.1002/ oa.1263.

Ionete C., Omojola M.F. MR angiographic demonstration of bilateral duplication of the extracranial vertebral artery: unusual course and review of the literature //Am. J. of Neuroradiology. - 2006. - Vol. 27. - P. 1304 - 1306.

Jitendra R., Hrishikesh J. Anatomical study of variation of vertebral artery entering the foramen transversarium of cervical vertebrae // National J. of Medical Research. - 2012. - Vol. 2. - P. 199 - 201.

Jovanovic M.S. A comparative study of the foramen transversarium of the sixth and seventh cervical vertebrae // Surgical Radiologic Anatomy. - 1990. - Vol. 12, iss. 3. - P. 167 - 172.

Kendi A.T. K., Brace J.R. Vertebral artery duplication and aneurysms: 64-slice multidetector CT findings // British J. of Radiology. - 2009. - Vol. 82. - P. e216-e228.

Kuzmin Y.V., Burr G.C., Jull A.T.J., Sulerzhitsky L.D. AMS 14C age of the Upper Palaeolithic skeletons from Sungir site, Central Russian Plain // Nuclear Instruments and Methods in Physics Research. Section B. - 2004. - Vol. 223/224. - P. 731 - 734.

Libby W. Radiocarbon Dating. - 2nd Ed. - Chicago: University of Chicago Press, 1955. - 175 p.

Marom A., McCullagh J.S.O., Higham T.F.G., Sinitsyn A.A., Hedges R.E.M. Single amino acid radiocarbon dating of Upper Paleolithic modern humans // Proceedings of the National Academy of Sciences USA. - 2012. - Vol. 109, N18. - P. 6878 - 6881.

Scheuer L., Black S. Developmental Juvenile Osteology. - L.: Academic Press, 2000. - 587 p.

Svensson A., Andersen K.K., Bigler M., Clausen H.B., Dahl-Jensen D., Davies S.M., Johnsen S.J., Muschler R., Parrenin E., Rasmussen S.O., Rothlisberger R., Seierstad L., Steffensen J.R, Vinther B.M. A 60000 year Greenland stratigraphic ice core chronology // Climate of the Past Discussions. - 2008. - Vol. 4. - P. 47 - 57.

Taitz C., Nathan H., Arensburg B. Anatomical observations of the foramina transversaria // J. of Neurology, Neurosurgery and Psychiatry. - 1978. - Vol. 41. - P. 170 - 176.

Tokuda K., Miyasaka K., Abe H., Takei H., Sugimoto S., Tsuru M. Anomalous atlantoaxial portions of vertebral and posterior inferior cerebellar arteries // Neuroradiology. - 1985. - Vol. 27. - P. 410-413.

Vasudeva N., Kumar R. Absense of foramen transversarium in human atlas vertebrae: A case report // Acta Anatomica. - 1995. - Vol. 152, N 3. - P. 230 - 233.

Webb W.S. Indian Knoll. - Knoxville: University of Tennessee Press, 1974. - 288 p.

Wickbom G.I., Williamson M.R. Anomalous foramen transversarium of C2 simulating erosion of bone // Neuroradiology. - 1980. - Vol. 19. - P. 43-45.

The article was submitted to the Editorial Board on 29.11.12, and the final version was published on 25.12.12.

page 131

Permanent link to this publication: